He is known for his capture of Sir William Wallace in 1305 and later joined with King Robert I of Scotland and received large land grants in Knapdale and Kintyre for his service.

With his older brother Alexander, John was involved in the resistance against King Edward I of England and were both captured after the Battle of Dunbar on 27 April 1296.

As sheriff of Dumbarton, in August 1305 John is alleged to have conspired with Aymer de Valence, 2nd Earl of Pembroke and Robert Clifford, 1st Baron Clifford, at the Parish Church in Rutherglen in Lanarkshire, to capture Sir William Wallace and have him handed over to the Captain of Scotland, below the Forth, John Segrave, 2nd Baron Segrave.

Wyntoun, whose Metrical Chronicle was written in 1418, says: Schyre Jhon of Menteith in tha days Tuk in Glasgow William Walays; And sent hym until Ingland sune, There was he quartayrd and undone.

A passage in the Scalachronica, quoted by John Leland, notes, "William Walleys was taken of the Counte of Menteith, about Glasgow, and sent to King Edward, and after was hanged, drawn, and quartered at London."

Menteith was nominated one of the representatives of the Scots barons in the parliament of both nations which assembled at London in September 1305 and was chosen upon the Scottish council, which was appointed to assist John of Brittany, the new Guardian of Scotland, in the English interest.

John was one of the negotiators of the thirteen years' truce between Bruce and the English, signed on 30 May 1323 and was present at a Scottish council at Berwick in June.